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Endothermy in the Solitary Bee Anthophora Plumipes: Independent Measures of Thermoregulatory Ability, Costs of Warm-Up and the Role of Body Size

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Endothermy in the Solitary Bee Anthophora Plumipes: Independent Measures of Thermoregulatory Ability, Costs of Warm-Up and the Role of Body Size JEB8628.q 26/10/98 5:56 pm Page 299 J. exp. Biol. 174, 299–320 (1993) 299 Printed in Great Britain © The Company of Biologists Limited 1993 ENDOTHERMY IN THE SOLITARY BEE ANTHOPHORA PLUMIPES: INDEPENDENT MEASURES OF THERMOREGULATORY ABILITY, COSTS OF WARM-UP AND THE ROLE OF BODY SIZE BY GRAHAM N. STONE* Oxford University Department of Zoology, South Parks Road, Oxford OX1 3PS Accepted 15 September 1992 Summary 1. This study examines variation in thoracic temperatures, rates of pre-flight warm-up and heat loss in the solitary bee Anthophora plumipes (Hymenoptera; Anthophoridae). 2. Thoracic temperatures were measured both during free flight in the field and during tethered flight in the laboratory, over a range of ambient temperatures. These two techniques give independent measures of thermoregulatory ability. In terms of the gradient of thoracic temperature on ambient temperature, thermoregulation by A. plumipes is more effective before flight than during flight. 3. Warm-up rates and body temperatures correlate positively with body mass, while mass-specific rates of heat loss correlate negatively with body mass. Larger bees are significantly more likely to achieve flight temperatures at low ambient temperatures. 4. Simultaneous measurement of thoracic and abdominal temperatures shows that A. plumipes is capable of regulating heat flow between thorax and abdomen. Accelerated thoracic cooling is only demonstrated at high ambient temperatures. 5. Anthophora plumipes is able to fly at low ambient temperatures by tolerating thoracic temperatures as low as 25˚C, reducing the metabolic expense of endothermic activity. 6. Rates of heat generation and loss are used to calculate the thermal power generated by A. plumipes and the total energetic cost of warm-up under different thermal conditions. The power generated increases with thoracic temperature excess and ambient temperature. The total cost of warm-up correlates negatively with ambient temperature. Introduction The majority of studies of endothermy in bees in temperate and cool climates have been on social species in the family Apidae, particularly in the genera Apis (e.g. Heinrich, 1979; Cooper et al. 1985; Dyer and Seeley, 1987; Coelho, 1991; Underwood, 1991) and Bombus (e.g. Heinrich, 1972a,b, 1976; Prys-Jones, 1986; Surholt et al. 1990; Esch and *Present address: NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks SL5 7PY. Key words: Anthophora plumipes, bee, thermoregulation, endothermy, energetics. JEB8628.q 26/10/98 5:56 pm Page 300 300 G. N. STONE Goller, 1991). Among solitary bees most studies have been on relatively large species active in warm or tropical climates, particularly the carpenter bees of the genus Xylocopa (Anthophoridae) (e.g. Chappell, 1982; Nicolson and Louw, 1982; Louw and Nicolson, 1983; Baird, 1986; Heinrich and Buchmann, 1986; Willmer, 1988; Surholt et al. 1990). Comparisons across species show that body mass alone is not a good indicator of endothermic ability (May, 1976) and small species adapted to cold thermal regimes are capable of high rates of warm-up and high thoracic temperatures (Stone and Willmer, 1989b). Endothermy is widespread among small solitary bees active in cool climates and is known in the families Andrenidae, Anthophoridae, Colletidae, Halictidae and Megachilidae (Stone and Willmer, 1989b). Do small solitary species have thermoregulatory abilities comparable with the better known social species active in similar environments? How do their responses to changes in ambient temperature, in terms of the thermal power generated and the total energetic cost of warm-up, compare to those of Bombus, the best known endothermic bees? This study addresses these questions through detailed study of a small anthophorid solitary bee, Anthophora plumipes, active in a cold thermal regime. Anthophora is a large genus of fast-flying, robust bees occurring on all continents except Australia and South America. They are often extremely furry and all members of the genus examined to date are extremely endothermic (G. Stone, in preparation). In Britain, the commonest species is Anthophora plumipes, whose geographic range extends as far as Israel in the east. In Britain, A. plumipes flies from March until May, and in Israel from February until April. Throughout its range it is active in the spring when weather conditions and ambient temperature (Ta) fluctuate widely. This variation creates a situation in which some degree of endothermic thermoregulation has advantages over activity that is governed solely by dependence on unpredictable environmental conditions. An important variable in studies of thermal physiology is body mass because, for organisms of a constant form, body mass determines surface area to volume ratios and hence the balance between mass-specific rates of heat generation and loss (May, 1976; Bartholomew, 1981; Heinrich and Heinrich, 1983). Across species, body mass is an important variable both in heterothermic insects (Stone and Willmer, 1989b; Coelho, 1991) and heterothermic mammals (Stone and Purvis, 1992). This study examines in detail the role of body size in warm-up rates and body temperatures in a single species. Materials and methods Field measurements of body temperature The ‘grab-and-stab’ techniques used in this study are as described by Stone and Willmer (1989a). Grab-and-stab measurements were made at feeding and nesting sites in the Botanical Gardens, Oxford, and in the grounds of Merton College and University College, Oxford, during 1987, 1988 and 1989. Laboratory measurements of body temperature were made at Oxford University Department of Zoology over the same period and at the Botany Department of the Hebrew University, Givat Ram, Jerusalem, in February and March 1989. In Israel, bees were collected from an artificial mediterranean JEB8628.q 26/10/98 5:56 pm Page 301 Endothermy in the solitary bee A. plumipes 301 plant community established at Beit Jala (Har Gilo) in the Occupied Territories of the West Bank to the south of Jerusalem. Laboratory measurement of warm-up rates and body temperatures During warm-up and tethered flight, the bee was suspended from a fine thermocouple implanted shallowly in the thoracic flight muscles, as described by Stone and Willmer (1989b). In bumblebees (Heinrich, 1972, 1976) and carpenter bees (Heinrich and Buchmann, 1986), the temperature of the thorax is controlled by regulation of heat transfer from the thorax in the form of hot haemolymph passing down the petiole into the abdomen. At low Ta, Bombus minimises heat loss from the thorax to the abdomen by operation of a countercurrent heat exchange system in the petiole (Heinrich, 1976). Continuous measurement of abdominal temperature (Tab) in A. plumipes was achieved using a flexible copper–constantan thermocouple (diameter 0.1mm) inserted through a small hole in the second abdominal tergite. The thermocouple was inserted dorso- laterally to avoid damage to the dorsal heart, to a depth of approximately 1mm, and secured in place with adhesive. The temperature at which a bee initiated tethered flight is referred to as its voluntary flight temperature (VFT). After flight for a period of 60s or so, body temperature usually stabilised at a value termed the stable flight temperature (SFT) (Stone and Willmer, 1989a). After each experiment, bees were released, apparently unharmed, at the site of capture. Laboratory investigations of thermogenesis were carried out at four ambient temperatures (Ta): 9, 16, 21 and 29˚C. After a number of warm-ups over the full range of thoracic temperature (Tth) from Ta to VFT, bees showed general lowering of warm-up rates. This apparent fatigue could be dramatically ‘cured’ by feeding the bee with a solution of sucrose. Shortly after feeding had been initiated, there was a marked increase in abdominal pumping and a rapid increase in Tth. The bee warmed to levels in excess of those in previous warm-ups and ceased feeding shortly before flight. This increase in apparent thermogenic ability remained for several subsequent warm-ups. The major effect of feeding was an increase in VFT and in the power of tethered flight. This suggests that observed levels of endothermy could be dependent on the energy reserves carried by the bee at the time of capture. Both male and female A. plumipes collect nectar to the exclusion of all other flight activities during the early part of their flying period (Stone, 1989). Bees were therefore collected during the later stages of this period to minimise the probability that they might be limited during warm-up by low levels of nectar in their crops. Each bee was also allowed only five periods of tethered flight before release. Conductance The rate at which a body cools depends on how rapidly heat is lost per unit area from its surface (its conductance, C) and on the temperature difference that exists between the body and its surroundings (for bees, the thoracic temperature excess, Tth2Ta, abbreviated to Tex). This relationship is expressed algebraically as: dTth/dt CTex. Conductance values can be calculated by multiplying the cooling constant [the gradient JEB8628.q 26/10/98 5:56 pm Page 302 302 G. N. STONE of a regression of cooling rate (y) on Tex (x)] determined by analysis of the cooling curve of each bee by the specific heat capacity of tissue (taken as 3.4Jg21 degree21; Heinrich, 1975; Coelho, 1991). In order to exclude the possibility of physiological modification of cooling rates, cooling constants were obtained for freshly killed dead bees. The bee was attached to a thermocouple in the normal way and its thorax heated with a microscope lamp (48W, Vickers, UK) situated 10cm from the bee. Heating of head and abdomen was minimised by shading them with pieces of polished sheet steel, acting both as shading screens and heat sinks. The bee was enclosed in a Perspex chamber to minimise the cooling effects of air currents in the room. When the bee’s thorax had been warmed to, and stabilised at, the required temperature, it was allowed to cool passively until it had equilibrated with room air temperature.
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